The oculomotor system
Or
Fear and Loathing at the Orbit
Michael E. Goldberg, M.D.
First you tell them what your gonna
tell them
• The phenomenology of eye movements.
• The anatomy and physiology of the
extraocular muscles and nerves.
• The supranuclear control of eye
movements: motor control and cognitive
plans.
The purposes of eye movements
• Keep an object on the fovea
 Fixation
 Smooth pursuit
• Keep the eyes still when the head moves
 Vestibulocular reflex
 Optokinetic reflex
• Change what you are looking at ( move the
fovea from one object to another)
 Saccade
• Change the depth plane of the foveal object
 Vergence – eyes move in different directions
The vestibuloocular reflex.
• The semicircular canals provide a head
velocity signal.
• The vestibuloocular reflex (VOR)
provides an equal and opposite eye
velocity signal to keep the eyes still in
space when the head moves.
The vestibular signal habituates, and is supplemented
by vision – the optokinetic response
Smooth pursuit matches eye
velocity to target velocity
Saccades move the fovea to a
new position
6 Muscles move the eyes
Levator Palpebrae
Superior Rectus
Lateral Rectus
Medial Rectus
Superior Oblique
Inferior Oblique
Inferior Rectus
How the single eye moves
• Horizontal:
 Abduction (away from the nose)
 Adduction (toward the nose).
• Vertical:
 Elevation (the pupil moves up)
 Depression (the pupil moves down)
• Torsional:
 Intorsion: the top of the eye moves towards the
nose
 Extorsion: the top of the eye moves towards the
ear.
The obliques are counterintuitive
• Each oblique inserts
behind the equator of
the eye.
• The superior oblique
rotates the eye
downward and intorts it!
• The inferior oblique
rotates the eye upward
and extorts it.
• Vertical recti tort the eye
as well as elevate or
depress it.
Oblique action depends on orbital
position
• The superior oblique
depresses the eye
when it is adducted
(looking at the
nose).
• The superior oblique
intorts the eye when
it is abducted
(looking towards the
ear)
3 Cranial Nerves Control the Eye
Levator Palpebrae
Superior Rectus
Inferior Rectus
Nerve III:
Oculomotor
Medial Rectus
Inferior Oblique
Superior Oblique
Lateral Rectus
Nerve IV:
Trochlear
Nerve VI:
Abducens
Left fourth nerve palsy
• Hyperopia in central
gaze.
• Worse on right gaze.
• Better on left gaze.
• Worse looking down to
right
• Better looking up to
right.
• Head tilt to right
improves gaze.
• Head tilt to left worsens
gaze.
Listing’s Law
• Torsion must be constrained or else vertical
lines would not remain vertical.
• Listing’s law accomplishes this: the axes of
rotation of the eye from any position to any
other position lie in a single plane, Listing’s
plane.
• This is accomplished by moving the axis of
rotation half the angle of the eye movement
The pulleys: something new in
orbital anatomy and physiology.
• How is Listing’s law accomplished?
• Extraocular muscles have two layers
 A global layer that inserts on the sclera
 An orbital layer that inserts on a collagen-elastin
structure between the orbit and globe. This
structure serves as a PULLEY through which the
global layer moves the eye.
• Moving the pulleys accomplish listings law.
(Demer).
Pulley Anatomy
The pulleys
Horizontal rectus pulleys change
their position with horizontal gaze.
Eye muscle nuclei
Mesencephalic
Thalamus
Reticular
Formation
Superior Colliculus
Inferior Colliculus
III
IV
Cerebellum
VI
Pontine
Nuclei
Vestibular Nuclei
Oculomotor neurons describe eye
position and velocity.
Lateral
Eye position – the step
Medial
Eye velocity – the pulse
Medial - Lateral
Eye Position
Abducens neuron
Sp/s
Pulse
Step
Neuron
Abducens neuron
The transformation from muscle
activation to gaze
• The pulse of velocity and the step of position
are generated independently.
• For horizontal saccades the pulse is
generated in the paramedian pontine reticular
formation.
• The step is generated in the medial vestibular
nucleus and the prepositus hypoglossi by a
neural network that integrates the velocity
signal to derive the position signal.
Horizontal saccades are generated in
the pons and medulla
Thalamus
Superior Colliculus
Inferior Colliculus
Medial
longitudinal
fasciculus
III
IV
Cerebellum
Paramedian
Pontine
Reticular
Formation
Pontine
Nuclei
VI
Vestibular Nuclei and
Nucleus Prepositus
Hypoglossi
Digression on Neural Integration
• Intuitively, you move your eyes from position to
position (the step).
• Higher centers describe a saccadic position error.
• The pontine reticular formation changes the
position error to a desired velocity (the pulse).
• The vestibulo-ocular reflex also provides the
desired velocity.
• In order to maintain eye position after the velocity
signal has ended, this signal must be
mathematically integrated.
Neurons involved in the generation
of a saccade
`
Generating the horizontal gaze
signal
• The medial rectus of one eye and the
lateral rectus of the other eye must be
coordinated.
• This coordination arises from
interneurons in the abducens nucleus
that project to the contralateral medial
rectus nucleus via the medial
longitudinal fasciculus.
Left lateral rectus
Abducens nerve
Paramedian
pontine reticular
formation
(saccade velocity)
Abducens
nucleus: motor
neurons and
interneurons.
Medial
vestibular
nucleus: eye
position, VOR
and smooth
pursuit velocity
.
Right medial rectus
Oculomotor
nucleus and
nerve: motor
neurons only
Medial
longitudinal
fasciculus
Nucleus prepositus
hypoglossi (eye
position)
To reiterate
• Ocular motor neurons describe eye position and velocity.
• For smooth pursuit and the VOR the major signal is the
velocity signal, which comes from the contralateral medial
vestibular nucleus.
• The neural integrator in the medial vestibular nucleus and
nucleus prepositus hypoglossi converts the velocity signal
into a position signal which holds eye position.
• For horizontal saccades the paramedian pontine reticular
formation converts the position signal from supranuclear
centers into a velocity signal.
• This signal is also integrated by the medial vestibular nucleus
and the nucleus prepositus hypoglossi.
• Abducens interneurons send the position and velocity signals
to the oculomotor nucleus via the medial longitudinal
fasciculus.
Vertical movements and vergence are
organized in the midbrain
Mesencephalic
Thalamus
Reticular
Formation
Posterior commissure
Superior Colliculus
Inferior Colliculus
rIMLF
III
Medial
Longitudinal
Fasciculus
Paramedian
Pontine
Reticular
Formation
Pontine
Nuclei
IV
Cerebellum
VI
Vestibular Nuclei
Internuclear ophthalmoplegia
• The medial longitudinal fasciculus is a
vulnerable fiber tract.
• It is often damaged in multiple sclerosis
and strokes.
• The resultant deficit is internuclear
ophthalmoplegia
• The horizontal version signal cannot
reach the medial rectus nucleus, but the
convergence signal can.
Supranuclear control of saccades
• The brainstem can make a rapid eye
movement all by itself (the quick phase
of nystagmus).
• The supranuclear control of saccades
requires controlling the rapid eye
movement for cognitive reasons.
• In most cases saccades are driven by
attention
Humans look at where they attend
Supranuclear control of saccades
Supplementary Eye Field
Posterior Parietal Cortex
Frontal Eye Field
Caudate Nucleus
Superior Colliculus
Substantia Nigra
Pars Reticulata
Reticular Formation
Supranuclear Control of Saccades
• Superior colliculus drives the reticular formation to
make contralateral saccades.
• The frontal eye fields and the parietal cortex drive the
colliculus.
• The parietal cortex provides an attentional signal and
the frontal eye fields a motor signal.
• The substantia nigra inhibits the colliculus unless
• It is inhibited by the caudate nucleus
• Which is, in turn, excited by the frontal eye field.
The effect of lesions
• Monkeys with collicular or frontal eye field lesions
make saccades with a slightly longer reaction time.
• Monkeys with combined lesions cannot make
saccades at all.
• Humans with parietal lesions neglect visual stimuli,
and make slightly hypometric saccades with longer
reaction times. Often their saccades are normal: if
they can see it they can make saccades to it.
• Humans with frontal lesions cannot make
antisaccades.
The Antisaccade Task
The Antisaccade Task
• Look away from a stimulus.
• The parietal cortex has a powerful signal
describing the attended stimulus.
• The colliculus does not respond to this signal.
• The frontal motor signal drives the eyes away
from the stimulus.
• Patients with frontal lesions cannot ignore the
stimulus, but must respond to the parietal
signal
Antisaccades
Supplementary Eye Field
Posterior Parietal Cortex
Frontal Eye Field
Caudate Nucleus
Superior Colliculus
Substantia Nigra
Pars Reticulata
Reticular Formation
Supranuclear control of pursuit: pursuit
matches eye velocity to target velocity
Frontal Eye Field
provides the trigger
to start the pursuit.
Middle temporal and middle
superior temporal (MT and MST)
provide the velocity signal
Striate Cortex
Dorsolateral
pontine nuclei
Vestibular
nucleus
Cerebellum vermis
and flocculus
Smooth pursuit
• Requires cortical areas that compute
target velocity, the dorsolateral pontine
nuclei, and the cerebellum.
• Utilizes many of the brainstem
structures for the vestibuloocular reflex
• Requires attention to the target.
Clinical deficits of smooth pursuit
• Cerebellar and brainstem disease
• Specific parietotemporal or frontal
lesions
• Any clinical disease with an attentional
deficit – Alzheimer’s or any frontal
dementia, schizophrenia